Neurodevelopment for syntactic processing distinguishes childhood stuttering recovery versus persistence

Abstract

Background: Characterized by the presence of involuntary speech disfluencies, developmental stuttering is a neurodevelopmental disorder of atypical speech-motor coordination. Although the etiology of stuttering is multifactorial, language development during early childhood may influence both the onset of the disorder and the likelihood of recovery. The purpose of this study was to determine whether differences in neural indices mediating language processing are associated with persistence or recovery in school-age children who stutter.

Methods: Event-related brain potentials (ERPs) were obtained from 31 6-7-year-olds, including nine children who do not stutter (CWNS), 11 children who had recovered from stuttering (CWS-Rec), and 11 children who persisted in stuttering (CWS-Per), matched for age, and all with similar socioeconomic status, nonverbal intelligence, and language ability. We examined ERPs elicited by semantic and syntactic (phrase structure) violations within an auditory narrative consisting of English and Jabberwocky sentences. In Jabberwocky sentences, content words were replaced with pseudowords to limit semantic context. A mixed effects repeated measures analysis of variance (ANOVA) was computed for ERP components with four within-subject factors, including condition, hemisphere, anterior/posterior distribution, and laterality.

Results: During the comprehension of English sentences, ERP activity mediating semantic and syntactic (phrase structure) processing did not distinguish CWS-Per, CWS-Rec, and CWNS. Semantic violations elicited a qualitatively similar N400 component across groups. Phrase structure violations within English sentences also elicited a similar P600 component in all groups. However, identical phrase structure violations within Jabberwocky sentences elicited a P600 in CWNS and CWS-Rec, but an N400-like effect in CWS-Per.

Conclusions: The distinguishing neural patterns mediating syntactic, but not semantic, processing provide evidence that specific brain functions for some aspects of language processing may be associated with stuttering persistence. Unlike CWS-Rec and CWNS, the lack of semantic context in Jabberwocky sentences seemed to affect the syntactic processing strategies of CWS-Per, resulting in the elicitation of semantically based N400-like activity during syntactic (phrase structure) violations. This vulnerability suggests neural mechanisms associated with the processing of syntactic structure may be less mature in 6-7-year-old children whose stuttering persisted compared to their fluent or recovered peers.

Keywords: Children; Event-related potentials; Language development; Language processing; N400; P600; Stuttering.

Figure 1

Grand average ERPs elicited by the semantic condition. ERPs of all participants in the CWNS, CWS-Rec, and CWS-Per groups reveal similar N400 waveforms elicited in the semantic canonical (black) and violation (red) conditions.

Figure 2

Grand average ERPs elicited by the syntactic condition within English sentences. ERPs of all participants in the CWNS, CWS-Rec, and CWS-Per groups reveal similar P600 waveforms elicited in the English syntactic canonical (black) and violation (red) conditions.

Figure 3

Grand average ERPs elicited by the syntactic condition within Jabberwocky sentences. ERPs of all participants in the CWNS, CWS-Rec, and CWS-Per groups, showing waveforms elicited in the Jabberwocky syntactic canonical (black) and violation (red) conditions.

Figure 4

Scalp map consisting of approximate locations for all electrodes included in analyses.

Figure 5

N400-like mean amplitude for the Jabberwocky syntactic condition. Group mean amplitude (μV) (600–900 ms) elicited by syntactic (phrase structure) violations within Jabberwocky sentences. Averaged across central-parietal electrodes (C3, CP3, P3, CZ, CPZ, PZ, C4, CP4, and P4), only CWS-Per show a larger negativity (N400-like effect) elicited by phrase structure violations relative to the canonical (negative plotted up).

Figure 6

N400-like effect distribution for the Jabberwocky syntactic condition. Scatterplot showing the distribution of mean amplitude (600–900 ms) differences (phrase structure violations minus canonical phrase structures) within Jabberwocky sentences, averaged across central-parietal electrodes (C3, CP3, P3, CZ, CPZ, PZ, C4, CP4, and P4). This distribution reveals the individual differences within the CWNS, CWS-Rec, and CWS-Per groups. Each datum represents a single child (negative plotted up).

Figure 7

P600 mean amplitude for the Jabberwocky syntactic condition. Group mean amplitude (μV) (1,200–1,500 ms) elicited by syntactic (phrase structure) violations within Jabberwocky sentences. Averaged across central-parietal electrodes (C3, CP3, P3, CZ, CPZ, PZ, C4, CP4, and P4), only CWNS and CWS-Rec show a larger positivity (P600) elicited by phrase structure violations relative to the canonical condition (negative plotted up).

Figure 8

P600 effect distribution for the Jabberwocky syntactic condition. Scatterplot showing the distribution of mean amplitude (1,200–1,500 ms) differences (phrase structure violations minus canonical phrase structures) within Jabberwocky sentences, averaged across central-parietal electrodes (C3, CP3, P3, CZ, CPZ, PZ, C4, CP4, and P4). This distribution reveals the individual differences within the CWNS, CWS-Rec, and CWS-Per groups. Each datum represents a single child (negative plotted up).